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Differential Connectivity of Perirhinal and Parahippocampal Cortices Within Human Hippocampal Subregions Revealed by High-Resolution Functional Imaging

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Differential Connectivity of Perirhinal and Parahippocampal Cortices Within Human Hippocampal Subregions Revealed by High-Resolution Functional Imaging 6550 • The Journal of Neuroscience, May 9, 2012 • 32(19):6550–6560 Behavioral/Systems/Cognitive Differential Connectivity of Perirhinal and Parahippocampal Cortices within Human Hippocampal Subregions Revealed by High-Resolution Functional Imaging Laura A. Libby,1 Arne D. Ekstrom,1,3 J. Daniel Ragland,2 and Charan Ranganath1,3 Departments of 1Psychology and 2Psychiatry and Behavioral Sciences and 3Center for Neuroscience, University of California, Davis, Davis, CA 95616 Numerous studies support the importance of the perirhinal cortex (PRC) and parahippocampal cortex (PHC) in episodic memory. Theories of PRC and PHC function in humans have been informed by neuroanatomical studies of these regions obtained in animal tract-tracing studies, but knowledge of the connectivity of PHC and PRC in humans is limited. To address this issue, we used resting-state functional magnetic resonance imaging to compare the intrinsic functional connectivity profiles associated with the PRC and PHC both across the neocortex and within the subfields of the hippocampus. In Experiment 1, we acquired standard-resolution whole-brain resting-state fMRI data in 15 participants, and in Experiment 2, we acquired high-resolution resting-state fMRI data targeting the hippocampus in an independent sample of 15 participants. Experiment 1 revealed that PRC showed preferential connectivity with the anterior hippocampus, whereas PHC showed preferential connectivity with posterior hippocampus. Experiment 2 indicated that this anterior–posterior functional connectivity dissociation was more evident for subfields CA1 and subiculum than for a combined CA2/ CA3/dentate gyrus region. Finally, whole-brain analyses from Experiment 1 revealed preferential PRC connectivity with an anterior temporal and frontal cortical network, and preferential PHC connectivity with a posterior medial temporal, parietal, and occipital network. These results suggest a framework for refining models of the functional organization of the human medial temporal lobes in which the PRC and PHC are associated with distinct neocortical pathways that, in turn, may differentially interact with regions along the anterior–posterior axis of the hippocampus. Introduction Burwell and Amaral, 1998a,b) (see Fig. 1A,B). However, because The medial temporal lobe (MTL) is a key component of a anatomical tracer studies are not feasible in humans, it is un- network of cortical and subcortical areas that are critical for known whether the human PRC and PHC exhibit differential memory (Squire and Zola-Morgan, 1991; Eichenbaum, 2006). connectivity with higher neocortical regions and with hippocam- These areas include the perirhinal cortex (PRC), parahip- pal subfields. pocampal cortex (PHC), entorhinal cortex (ERC), and hip- Functional connectivity analysis of blood oxygenation level- pocampal formation (HF), which contains subfields cornu dependent (BOLD) functional magnetic resonance imaging (fMRI) ammonis 1–3 (CA1, CA2, CA3), dentate gyrus (DG), and provides a noninvasive means to assess in vivo large-scale connectiv- subiculum (Lorente de No, 1934; Duvernoy and Bourgouin, ity in the human brain (Raichle et al., 2001; Biswal et al., 2010). 1998). Lesion and human neuroimaging studies suggest distinct Coherent low-frequency signal fluctuations recorded during roles for the PRC and PHC in memory formation and retrieval, resting-state fMRI reflect broad networks of brain regions linked although it is not clear how best to characterize these roles by direct and indirect anatomical connections (Vincent et al., (Brown and Aggleton, 2001; Davachi, 2006; Eichenbaum et al., 2007; Skudlarski et al., 2008; Greicius et al., 2009; Honey et al., 2007; Ekstrom and Bookheimer, 2007; Litman et al., 2009; Ran- 2009; Barnes et al., 2010). To our knowledge, only one previous ganath, 2010). Some clues come from tract-tracing studies in study (Kahn et al., 2008) has specifically examined intrinsic func- rodents and monkeys suggesting that PRC and PHC differ in tional connectivity with human PHC and PRC. The posterior their anatomical connectivity with sensory and association areas hippocampus and PHC showed significant functional connectiv- and with hippocampal subfields (Suzuki and Amaral, 1994a,b; ity with retrosplenial cortex and medial and ventrolateral parietal areas, whereas anterior hippocampus and a combined PRC–ERC region showed significant functional connectivity with anterior Received July 20, 2011; revised Feb. 23, 2012; accepted March 18, 2012. Authorcontributions:L.A.L.,A.D.E.,J.D.R.,andC.R.designedresearch;L.A.L.performedresearch;A.D.E.contrib- and ventrolateral temporal cortex. However, the spatial resolu- uted unpublished reagents/analytic tools; L.A.L. analyzed data; L.A.L., A.D.E., J.D.R., and C.R. wrote the paper. tion of standard whole-brain fMRI cannot resolve BOLD signal ThisworkwassupportedbyNationalInstitutesofHealthGrantsR01MH084895andRO1MH83734andtheAlfred differences across different HF subfields, which have dimensions T. Sloan Foundation. We gratefully acknowledge Dr. Steve Petersen for the helpful suggestions. on the order of millimeters and may contain discrete connectivity Correspondence should be addressed to Laura A. Libby, University of California, Davis, Center for Neuroscience, 1544 Newton Court, Davis, CA 95616. E-mail: [email protected]. patterns not detectable at the larger scale. Newly developed high- DOI:10.1523/JNEUROSCI.3711-11.2012 resolution fMRI techniques centered on the MTL have revealed Copyright © 2012 the authors 0270-6474/12/326550-11$15.00/0 distinct patterns of activity in different HF subfields during task Libby et al. • Human PRC and PHC Functional Connectivity J. Neurosci., May 9, 2012 • 32(19):6550–6560 • 6551 Figure 1. Medial temporal lobe anatomical parcellation. A, B, Model of cortical and hippocampal connectivity of PRC and PHC with neocortex (A) and hippocampal subfields (B) based on animal anterograde and retrograde tracer studies (Burwell, 2000). C, Examples of individually defined ROIs for PRC and PHC for a single subject in Experiment 1. D, Examples of individually defined ROIs for PRC, PHC, ERC, CA1, CA2/CA3/DG, and subiculum in Experiment 2. (Ekstrom et al., 2009; Suthana et al., 2010; Dudukovic et al., slices; voxel size, 1 ϫ 1 ϫ 1 mm). Images sensitive to BOLD contrast were 2011), but this method has not been applied to questions about acquired using a gradient echo planar imaging (EPI) sequence (210 time resting-state functional connectivity in the MTL. points; matrix size, 64 ϫ 64; TR, 2000 ms; TE, 25 ms; FOV, 220; 34 slices, ϫ ϫ Here, we report results from two experiments examining in- interleaved; voxel size, 3.4375 3.4375 3.4 mm) for 7 min while trinsic functional networks correlated with signal in PHC and participants rested with eyes open and lights on a low setting. The FMRI Expert Analysis Tool in the FMRIB Software Library (FSL PRC seed regions. In Experiment 1, we used standard-resolution version 4.1; www.fmrib.ox.ac.uk/fsl) was used for fMRI analysis. Brain resting-state fMRI to identify distributed whole-brain networks volumes were extracted from full-head functional and structural images. showing preferential functional connectivity with individually Functional images were motion corrected and bandpass filtered for fre- anatomically defined PHC and PRC seed regions. In Experiment quencies of 0.01–0.1 Hz. To prepare volumes for time course extraction, 2, we used high-resolution resting-state fMRI to characterize functional images were registered to each participant’s MPRAGE image functional connectivity between PHC and PRC seeds with ante- using a rigid-body transformation (df ϭ 6) using FMRIB’s Linear Image rior versus posterior sections of HF subfields (subiculum, CA1, Registration Tool (FLIRT) (Jenkinson and Smith, 2001; Jenkinson et al., and CA2/CA3/dentate gyrus). 2002). Demarcations of anatomical regions of interest. Boundaries between Materials and Methods PHC and PRC were defined manually on individual participant Participants native-space MPRAGE images in FSLView using criteria outlined by Two independent samples of 15 young, healthy adults underwent whole- Insausti et al. (1998), Duvernoy and Bourgouin (1998) and Zeineh et brain (eight females) or high-resolution (eight females) fMRI scanning. al. (2001). PHC regions of interest (ROIs) extended from the first slice Participants were excluded for current use of psychoactive drugs and containing the body of the hippocampus to the slice halfway through history of head trauma or neurologic or psychiatric illness. Informed the lateral ventricles in the anterior–posterior direction, and from the consent was obtained before MRI scanning. collateral sulcal fundus to the most medial vertex of the parahippocam- pal gyrus in the lateral–medial direction. PRC ROIs extended from the Experiment 1: whole-brain imaging most anterior slice of the collateral sulcus to the last slice containing the Data acquisition and preprocessing. Participants underwent scanning at hippocampal head in the anterior–posterior direction and across both the UC Davis Imaging Research Center on a 3T Siemens Trio system banks of the collateral sulcus in the lateral–medial direction. PHC and (Siemens) with an eight-channel phased-array head coil (N ϭ 15; two PRC ROIs for right and left hemispheres were created separately by man- subjects were scanned after a system upgrade to the Total imaging matrix ual tracing of gray matter within these demarcations (Fig. 1C). To reduce (Tim) acquisition system, but the resulting images
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